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Eileen Hebets Publications Papers in the Biological Sciences

4-2009

Tactile learning by a whip spider, marginemaculatus C. L. Koch (Arachnida, )

Roger D. Santer University of Limerick, Ireland, [email protected]

Eileen Hebets University of Nebraska - Lincoln, [email protected]

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Santer, Roger D. and Hebets, Eileen, "Tactile learning by a whip spider, C. L. Koch (Arachnida, Amblypygi)" (2009). Eileen Hebets Publications. 47. https://digitalcommons.unl.edu/bioscihebets/47

This Article is brought to you for free and open access by the Papers in the Biological Sciences at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Eileen Hebets Publications by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Published in Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 195:4 (April 2009), pp. 393-399; doi: 10.1007/s00359-009-0417-8 Copyright © Springer-Verlag 2009. Used by permission. Submitted October 27, 2008; revised January 12, 2009; accepted January 16, 2009; published online February 7, 2009.

Tactile learning by a whip spider, Phrynus marginemaculatus C. L. Koch (Arachnida, Amblypygi)

Roger D. Santer1, 2 and Eileen A. Hebets1

1. School of Biological Sciences, University of Nebraska–Lincoln, Lincoln, NE 68588, USA 2. Department of Life Sciences, Schrödinger Building, University of Limerick, Limerick, Ireland Corresponding author — Roger D. Santer, email [email protected]

Abstract The ability of to learn and remember underpins many behavioral actions and can be crucial for survival in certain contexts, for example in finding and recognizing a habitual refuge. The sensory cues that an learns in such situations are to an extent determined by its own sensory specializations. Whip spiders (Arachnida, Ambly- pygi) are nocturnal and possess uniquely specialized sensory systems that include elongated “antenniform” forelegs specialized for use as chemo- and mechanosensory feelers. We tested the tactile learning abilities of the whip spi- der Phrynus marginemaculatus in a maze learning task with two tactile cues of different texture—one associated with an accessible refuge, and the other with an inaccessible refuge. Over ten training trials, whip spiders got faster and more accurate at finding the accessible refuge. During a subsequent test trial where both refuges were inaccessible, whip spiders searched for significantly longer at the tactile cue previously associated with the accessible refuge. Using high-speed cinematography, we describe three distinct antenniform leg movements used by whip spiders during tac- tile examination. We discuss the potential importance of tactile learning in whip spider behavior and a possible role for their unique giant sensory neurons in accessing tactile information. Keywords: texture discrimination, associative learning, giant neuron, orientation, mechanoreception Abbreviations: CS = Conditioned stimulus; fps = frames per second; GN = Giant neuron

Introduction 1998; Collett and Collett 2002). However, environmental features provide sensory cues across many modalities, Learning allows an animal to modify its behavior in and the ones learned and exploited by an animal for the accordance with current environmental conditions. This guidance of its behavior will likely reflect its own sen- ability can be crucial for survival, for example when sory specializations (e.g. Dyer 1998). toxic foods must be avoided after exposure or habitual Whip spiders, non-spider in the order Am- shelters and/or food sources found and returned to. blypygi, are interesting from this point of view since Many animals that shelter or forage repeatedly in par- they are nocturnal and possess uniquely specialized sen- ticular locations find and recognize these locations (or sory systems highly adapted for the reception of chemo- goals), using strategies that incorporate learned asso- and mechanosensory cues. Walking on only their ciations between the goal itself and sensory cues from posterior three pairs of legs, their first pair of legs (‘an- permanent or reliable environmental features (e.g. Shet- tenniform legs’) are enormously elongated (2.5× their tleworth 1998). For many , visual and olfactory body length in some species but much longer in others), cues are of particular importance for these purposes and specialized for a sensory function. These antenni- (e.g. Dittman and Quinn 1996; Dyer 1998; Shettleworth form legs are covered with many types of chemo- and

393 394 Santer & Hebets in Journal of Comparative Physiology A 195 (2009) mechanosensory sensilla (Igelmund 1987), and contain males and six females) collected from Big Pine Key, at least seven unique giant neurons that carry mechano- FL, USA in August 2006. Whip spiders were individu- sensory information rapidly from these sensilla to the ally housed under a reversed 12:12 hour light cycle in central nervous system (Igelmund and Wendler 1991a,b; 100 mm × 100 mm × 125 mm plastic boxes. Humidity Spence and Hebets 2007). When active, whip spiders was maintained using water-soaked cotton wicks that constantly probe the area around them with their an- also allowed access to water, and whip spiders were tenniform legs both when walking and when stationary fed one cricket twice per week. Experiments were con- (regardless of illumination conditions), and the antenni- ducted in August 2007. form legs are considered the most important structures for spatial orientation (Weygoldt 2000). Experimental arena Many whip spiders reliably inhabit particular ref- uges during the day and return to them after forag- Experiments were conducted in a circular plastic ing at night. Individual Phrynus pseudoparvulus (de Ar- arena with two slits cut in the floor (Figure 1a). A dark- mas and Víquez 2001) occupy particular tree crevices ened 85 mm × 85 mm × 60 mm plastic box was placed or buttresses at the base of trees during the day, but beneath each slit as a refuge. The arena was lit from leave them to forage at night (Hebets 2002); individ- above using a fiber optic lamp (FO-150 “Lumina,” Chiu ual Heterophrynus batesii and H. longicornis reside on Technical Corporation, Kings Park, NY, USA) with a the same tree for weeks or months, occasionally leav- light guide positioned approximately 300 mm above ing the tree to forage at night but returning before dawn each arena floor slit. This strongly illuminated the arena (Beck and Görke 1974; Weygoldt 1977). Whip spiders [1,400 lux, measured using a VWR Scientific dual range can also orient to their refuges when artificially dis- light meter (model 62344-944), West Chester, PA, USA], placed from them: H. batesii displaced up to 10 m from but left each refuge dark. Each refuge was marked with their home tree can navigate back to it, within one night a tactile cue: a 100 mm × 50 mm sandpaper patch sur- for displacements <7.5 m (Beck and Görke 1974; Wey- rounding the slit and a 10 mm × 60 mm sandpaper wall goldt 2000). It has been hypothesized that sensory cues along the side of the slit closest to the arena wall (Fig- (particularly olfactory cues) received by the antenni- ure 1b). Tactile cues were made from aluminum oxide form legs are important in this context since removing sandpaper (Norton Abrasives, Worcester, MA, USA); the distal tips of a whip spider’s antenniform legs pre- one tactile cue had a coarse texture (P36, average parti- vented it from returning to its refuge after being dis- cle diameter 538 μm), the other a fine texture (P400, av- placed (Beck and Görke 1974; Weygoldt 2000). erage particle diameter 35 μm). Tactile cues were spray- Since the antenniform legs of whip spiders are spe- painted flat black (Quick Color Spray Enamel, Roc Sales cialized for the reception of mechanosensory cues as Inc., Vernon Hills, IL, USA) to minimize visual differ- well as chemosensory ones, in this study we wanted to ences between them. After painting, the experimenter investigate whether the whip spider P. marginemaculatus could easily distinguish the different tactile cues on the C. L. Koch is capable of tactile learning. Specifically, we basis of touch. investigated whether this species could learn to associ- ate a tactile proximal cue with a refuge. Individual P. Training trials marginemaculatus are reliably found beneath particular ‘home’ limestone rocks in the pine rock hammock of the During training trials, the entrance to one refuge was Florida Keys during the day, but leave these refuges to accessible and the other was inaccessible (the entrance forage at night (E. A. Hebets, unpublished). These rocks to the inaccessible refuge was covered with a plas- vary in size, shape, and surface texture (R. D. Santer and tic mesh that prevented a whip spider from entering). E. A. Hebets, personal observation). As such, tactile cues Whip spiders were divided into two groups of six (three received by the antenniform legs are a potential source males and three females). For one group the accessible of information that P. marginemaculatus could exploit in refuge was always associated with the coarse textured orienting to, and recognizing its home rock, as well as tactile cue, for the other it was always associated with for the more general guidance of behavior. the fine textured tactile cue. We refer to the tactile cue associated with the accessible refuge as CS+ (CS = con- ditioned stimulus), and the one associated with the in- Materials and methods accessible refuge as CS−. Tactile cues were randomly as- signed a side of the arena for each trial to prevent side We investigated whether whip spiders could learn to effects or external landmarks indicating refuge identity associate a tactile proximal cue with a refuge using aver- or position. sive strong lighting conditions during the dark phase For each whip spider, ten training trials were con- of their light cycle as motivation. We performed exper- ducted over consecutive days to mimic the frequency iments on 12 adult P. marginemaculatus C. L. Koch (six of nightly foraging trips (E. A. Hebets, unpublished). Tactile learning by a whip spider, Phrynus marginemaculatus C. L. Koch 395

Figure 1. Arena for training and test trials. a.) The arena was an opaque circular plas- tic container with two refuge entrances cut in the floor. Ref- uge entrances were marked with coarse and fine texture tactile cues (represented by different shading). b.) Both the coarse and fine texture tactile cues were sandpaper patches surrounding a refuge en- trance and a 1-cm high sand- paper wall behind it. Both tac- tile cues were spray-painted flat black.

Training trials were conducted during the dark phase of perimentation. Ten animals remained for data analysis the whip spiders’ light cycle (their normal active phase). (three females and two males in the coarse CS+ group, In each trial, whip spiders were placed in the centre and two females and three males in the fine CS+ group). of the arena under an upturned glass vial which was However, we noted no differences between the perfor- slowly lifted. From this position both tactile cues were mance of males and females, or animals in the different within reach of the antenniform legs. Due to their noc- CS+ texture groups in our experiments. turnal habits, whip spiders were highly motivated to escape the strong lighting of the arena by entering one Test trials of the two darkened refuges. Training trials lasted un- til a whip spider entered the accessible refuge associated Test trials were carried out on the day following the with the CS+ tactile cue. Where this did not occur within last training trial. As in training trials, tactile cues were 1 h, an acetate screen was introduced to direct the whip randomly assigned to an arena side, but both refuge en- spider towards CS+ and the accessible refuge, where it trances were blocked with black plastic mesh screen- would eventually enter. This was usually only neces- ing. Whip spiders were introduced into the centre of sary during the first one or two training trials. After a the arena as in training trials and observed for 45 min. training trial, a whip spider was returned to its normal We recorded (1) the first choice of refuge (defined as the housing under normal dark illumination. The arena, ref- first refuge entrance intensively explored by the whip uges, and screening were cleaned with 100% ethanol to spider); (2) the amount of time a whip spider spent with remove chemical residues and the tactile cues were dis- any part of its body in contact with each tactile cue; carded (new cues were used for each training trial). and (3) the amount of time a whip spider spent actively During training trials we recorded (1) the time of first probing a tactile cue with its antenniform legs. Time movement; (2) the time taken for a whip spider to en- contacting and probing the tactile cues was converted ter the accessible refuge from the start of the trial (la- to an index calculated as the fraction of total time a be- tency); and (3) whether its first choice of refuge was cor- havior was performed that it was directed at CS+ minus rect (defined as entering the accessible refuge without the fraction of time it was directed at CS−. Positive val- having intensively explored the entrance to the inacces- ues indicate searches directed at CS+ and negative val- sible one). ues indicate searches directed at CS−. During training trials, two whip spiders (a female in the fine CS+ group and a male in the coarse CS+ group) High-speed cinematography which appeared to be learning the task stopped com- pleting it and instead remained motionless during sev- After completion of learning experiments we filmed eral consecutive days of training trials. This behav- the antenniform leg movements of five whip spiders ior was later determined to be associated with molting as they examined pieces of filter paper attached to the and these individuals were excluded from further ex- walls of an 85 mm × 85 mm × 60 mm plastic box. Films 396 Santer & Hebets in Journal of Comparative Physiology A 195 (2009) were captured at 60 or 500 fps using a Fastcam 1024PCI high-speed digital camera (Photron USA, San Diego, CA, USA) and additional lighting was as for learning experiments.

Statistical analysis of data

Statistical analyses were carried out in SPSS v.15 for Windows (Systat Software Inc., San Jose, CA, USA) or by hand after Zar (1999). Shapiro–Wilk tests identified several cases where data differed significantly from a normal distribution, and sample sizes were relatively small. As such, we employed non-parametric statistical methods throughout.

Results

General behavior

In preliminary observations whip spiders showed lit- tle interest in either tactile cue and spent most of their time circling the wall of the arena, intensively examin- ing it with their antenniform legs. When they encoun- tered a tactile cue, they briefly examined it with their antenniform legs, but then directed their search effort back at the arena wall. We presume that these examina- tions were an attempt to find an exit to the arena and be- Figure 2. Evidence of tactile learning during training trials. a.) cause they were not directed preferentially at the tactile Over the ten training trials, mean latency to refuge entrance cues, an innate association between these cues and a ref- decreased (filled circles, solid line). This effect was due to a re- duction in search time since there was no relationship between uge location is unlikely. training trial number and the mean time that whip spiders be- gan searching in each trial (open circles, dashed line). b.) Over Training trials ten training trials, the number of whip spiders making a cor- rect first choice of refuge increased. Data are from ten whip Whip spiders never entered a refuge without first ex- spiders, for five CS+ was coarse textured, for five CS+ was fine amining the surrounding tactile cue with their antenni- textured. Bars are SEM. form legs. Over the course of ten training trials, latency to entering the accessible refuge decreased (Figure 2a, filled circles). There was a significant effect of training correct first choice of refuge was correlated with train- trial number on latency to accessible refuge entrance ing trial number, indicating increasing accuracy over (Friedman test, χ2 = 27.54, df = 9, P = 0.001) and there the ten trials [Figure 2b; Spearman’s rank correlation co- was a significant decrease in latency between train- efficient, (r s)c = 0.732, n = 10, P < 0.05]. ing trial one and ten (paired-sample, one-tailed Wil- coxon signed ranks test, T− = 0, n = 10, P < 0.0025). Al- Test trials though whip spiders frequently freeze when confronted with novel or threatening stimuli (Weygoldt 2000; R. D. During test trials, eight out of ten whip spiders cor- Santer and E. A. Hebets, personal observation), their de- rectly chose the CS+ refuge first, although this distri- creasing latency to accessible refuge entrance over the bution of choices did not differ significantly from ran- training trials was not due to less time spent in freezing dom (Chi-square goodness-of-fit test, χ2 = 3.6, df = 1, behavior at the start of later trials: We could not detect a P = 0.058). However, whip spiders’ searches were pref- difference between movement start times across training erentially directed at the CS+ tactile cue: the indices de- trials (Figure 2a, open circles; Friedman test, χ2 = 9.12, scribing (1) contact with the tactile cues, and (2) probing df = 9, P = 0.426), or between movement start times in of the tactile cues with the antenniform legs (calcu- training trials one and ten (paired-sample, two-tailed lated as the fraction of time a behavior was directed at Wilcoxon signed ranks test, T = 19.5, n = 10, P < 0.50). CS+ minus the fraction of time it was directed at CS−) Furthermore, the number of whip spiders making a were both significantly greater than 0 (contact index: one- Tactile learning by a whip spider, Phrynus marginemaculatus C. L. Koch 397

High-speed cinematography

Since whip spiders always examined tactile cues with their antenniform legs before trying to enter a refuge, tactile information is likely accessed using the antenniform legs. High-speed films of examina- tion behaviors revealed three characteristic antenni- form leg movements—‘tip touches’, ‘flat touches’, and ‘tip scrapes’ (Figure 4). During tip touches, the anten- niform leg tip was quickly tapped against the surface being examined. During flat touches, the distal half of the antenniform leg tarsus was held against the sur- face; and during tip scrapes the antenniform leg tip was dragged across the surface with a pronounced bend at the mid-point of the tarsus. Of 12 tip scrapes recorded, the mean length of substrate over which the antenniform leg tip was scraped was 1.55 ± 0.27 mm (SEM), and the mean speed at which it was scraped was 0.018 ± 0.003 ms−1 (SEM).

Discussion

Here we have shown that the whip spider P. mar- ginemaculatus can learn to associate a tactile cue with a Figure 3. During test trials, whip spiders spent longer search- refuge. Over the course of ten training trials, the whip ing the CS+ tactile cue. Plot shows the fraction of search time spiders’ latency to refuge entrance decreased and the whip spiders spent probing the positively conditioned tactile cue (CS+) with their antenniform legs, minus the fraction of number of animals making the correct first refuge choice time they spent probing the non-conditioned tactile cue (CS−). increased. In the test trial where both refuges were inac- Positive values indicate that the majority of search effort was di- cessible, whip spiders directed their search effort at the rected at the positively conditioned tactile cue. Box indicates tactile cue previously associated with the accessible ref- the 25th and 75th percentiles, black bisecting line is the median, uge during training trials. grey bisecting line is the mean. Whiskers indicate 5th and 95th Tactile learning has previously been demonstrated percentiles. Asterisks indicate a significant difference (P < 0.01) for several other invertebrate species. The tactile prop- from 0 (see text). Data are from ten whip spiders. erties of flower petals are used by Manduca sexta to lo- cate nectar using its proboscis (Goyret and Raguso sample, one-tailed Wilcoxon signed ranks test against 2006) and can be learned by bees (Kevan and Lane

M0 = 0, T− = 10, n = 10, P < 0.05; probing index: one- 1985; Erber et al. 1998). During goal orientation, the sample, one-tailed Wilcoxon signed ranks test against desert ant, Cataglyphis fortis (a predominantly visual

M0 = 0, T− = 4, n = 10, P < 0.01; Figure 3). navigator), can learn tactile properties of the ground

Figure 4. Antenniform leg movements during the examination of surfaces. During surface examination, three types of antenni- form leg movement were evident: a.) ‘Tip touches’—the tip of the antenniform leg is tapped against the surface being examined; b.) ‘Flat touches’—the entire antenniform leg tarsus distal to the bend at its mid-point is held against the surface being examined; c.) ‘Tip scrapes’—the tip of the antenniform leg is scraped across the surface being examined. Note the pronounced bend, proxi- mal to articles 22/23 of the tarsus. All films were made at 60 fps. 398 Santer & Hebets in Journal of Comparative Physiology A 195 (2009) as navigational landmarks, and both textural and vi- behavior, regardless of whether visual cues can also be sual properties of a landmark must be in agreement for exploited (Weygoldt 2000). the ant to use it (Seidl and Wehner 2006). The ability A unique feature of whip spider antenniform legs is of P. marginemaculatus to learn tactile cues and associ- that they contain an array of giant sensory neurons with ate them with a refuge might be useful during its noc- no known behavioral function (Igelmund and Wendler turnal orientation to, and recognition of home rocks in 1991a). Of the neurons with characterized response its natural environment. The very long antenniform properties, giant interneurons GN1 and 2 respond to legs of P. marginemaculatus (approximately 2.5 body mechanosensory stimulation of the bristle hairs on char- lengths) would allow such tactile cues to be accessed at acteristic areas of the antenniform leg tarsus, and gi- a distance, increasing their potential usefulness in this ant sensory neurons GN6 and 7 (which are believed to context (e.g. Weygoldt 2000). be either receptor cells of a slit sense organ or putative In our experiments we minimized visual differences joint receptor cells) respond to bending around a partic- between stimuli, but we cannot completely rule out the ular joint (around tarsal articles 22/23) in the mid-tar- possibility that the whip spiders could distinguish them sus (Igelmund and Wendler 1991a,b; Spence and Hebets visually (since learning was motivated by aversive illu- 2007). Here, high-speed cinematography revealed three mination conditions, our experimental design did not movements by the antenniform legs during surface ex- permit experiments with blindfolded whip spiders). amination that appear well matched to these response However, visual discrimination (or at least solely visual properties and hint at a potential role for the giant neu- discrimination) is unlikely since whip spiders examined rons in coding textural information. Tip touches seem the texture patches using intensive probes of their an- suited to defining the physical limits (shape) of an ob- tenniform legs, normally standing on the texture patch ject and this information could be signaled by activity where the dorsal placement of their eyes would not af- in GN1 which is excited by mechanical stimulation of ford close visual examination of the patches. Before en- the antenniform leg tip (Igelmund and Wendler 1991a, tering a refuge, a whip spider always examined the b). Flat touches bring a large area of the tarsus into con- surrounding texture patch with its antenniform legs, in- tact with the surface being examined, and may maxi- dicating that tactile examination was required for patch mize the number of contact chemoreceptive bristle hairs identification, rather than visual examination from a on the antenniform leg in contact with the surface be- distance alone. ing examined (Igelmund 1987; Foelix and Hebets 2001). Outside of the laboratory, the nocturnal activity of The overlapping receptive fields of GN1 and 2 across P. marginemaculatus might be predicted to minimize the the whole tarsus could be useful in positioning the an- usefulness of visual cues. However, a tropical noctur- tenniform leg during these movements (Igelmund and nal bee and desert wandering spider have been shown Wendler 1991a, b). During tip scrapes the antenniform to exploit visual cues for goal orientation even under leg tip is dragged across the surface being examined extreme low light conditions (Warrant et al. 2004; Nør- with a pronounced bend proximal to the joint between gaard et al. 2008). In the case of the wandering spider, tarsal articles 22/23. Flexion about this joint excites GN6 relatively large lenses and a combination of temporal and 7 (Igelmund and Wendler 1991a; Spence and He- and spatial summation are hypothesized to allow it to bets 2007), and such flexions could result from the an- salvage a coarse visual sensitivity for landscape features tenniform leg tip being deflected by surface irregular- in its desert environment (Nørgaard et al. 2008). In these ities during a scrape, allowing the GN6/7 response to spiders, the eyes that function in nocturnal navigation code textural information. A similar mechanism of tex- have mean lens diameters of 470 μm (anterior median ture coding has been found in sensory pathways from eyes), 330 μm (anterior lateral eyes), and 430 μm (pos- rat whiskers (e.g. Arabzadeh et al. 2003). terior lateral eyes), whilst the posterior median eyes Previous studies have demonstrated the olfactory (which do not function in nocturnal navigation) have sensitivity of sensilla on the antenniform legs of whip lens diameters of 280 μm (Nørgaard et al. 2008). By con- spiders and hypothesized that they play important roles trast, the lenses of P. marginemaculatus are very much in the guidance of natural behavior (Hebets and Chap- smaller than those of the wandering spider—from an man 2000; Hebets 2002). Here we have also provided adult male used in this study we measured the diameter the first demonstration of tactile learning in a whip spi- of one median eye lens as 167 μm, and the diameter of der, indicating the potential usefulness of tactile cues in one lateral eye lens as 191 μm—indicating that they may the same context. Both modalities could be of consider- not be as effective at capturing sufficient light for good able usefulness during activities such as finding and rec- vision at night. However, little is known about whip ognizing a habitual refuge at night. Whip spiders may spider eyes and future study is necessary to establish prove to be excellent models for understanding the tac- their true visual sensitivity. Nevertheless, the uniquely tile guidance of behavior, but field studies are now re- adapted antenniform legs of whip spiders indicate that quired to investigate the true importance of these abili- they play an important role in the guidance of natural ties in natural behavior. Tactile learning by a whip spider, Phrynus marginemaculatus C. L. Koch 399

Acknowledgments — We thank the U.S. Fish and Wildlife Hebets EA, Chapman RF (2000) Electrophysiological stud- Service and National Key Deer Refuge for permitting whip ies of olfaction in the whip spider Phrynus parvulus spider collection; D. P. Franklin for help conducting prelimi- (Arachnida, Amblypygi). J Insect Physiol 46:1441–1448 nary observations; K. A. Swoboda for animal care; D. J. Wilg- Igelmund P (1987) Morphology, sense organs and regen- ers for calibrating illumination in our experimental arena; and eration of the forelegs (whips) of the whip spider Het- R. M. Adams, K. D. Fowler-Finn, A. S. Rundus, S. K. Schwartz, erophrynus elaphus (Arachnida, Amblypygi). J Morphol C. A. Wei, D. J. Wilgers, and R. H. Willemart for comments on 193:75–89 this manuscript. This work was funded by a Searle Founda- tion Scholars grant to E. A. Hebets. These experiments comply Igelmund P, Wendler G (1991a) The giant fiber system in with the “Principles of animal care,” publication No. 86-23, re- the forelegs (whips) of the whip spider Heterophry- vised 1985 of the National Institutes of Health, and also with nus elaphus Pocock (Arachnida: Amblypygi). J Comp the current laws of the United States of America. Physiol A 168:63–73 Igelmund P, Wendler G (1991b) Morphology and phys- References iology of peripheral giant interneurons in the forelegs (whips) of the whip spider Heterophrynus elaphus Pocock Arabzadeh E, Petersen RS, Diamond ME (2003) Encod- (Arachnida: Amblygi). J Comp Physiol A 168:75–83 ing of whisker vibration by rat barrel cortex neurons: Kevan PG, Lane MA (1985) Flower petal microtex- Implications for texture discrimination. J Neurosci ture is a tactile cue for bees. Proc Natl Acad Sci USA 23:9146–9154 82:4750–4752 Beck L, Görke K (1974) Tagesperiodik, revierverhalten und Nørgaard T, Nilsson D-E, Henschel JR, Garm A, Wehner beutefang der geisselspinne Admetus pumilio C. L. Koch R (2008) Vision in the nocturnal wandering spider Leu- im freiland. Z Tierpsychol 35:173–186 corchestris arenicola (Araneae: Sparassidae). J Exp Biol Collett TS, Collett M (2002) Memory use in insect visual 211:816–823 navigation. Nat Rev Neurosci 3:542–552 Seidl T, Wehner R (2006) Visual and tactile learn- de Armas LF, Víquez C (2001) Nueva especie de Phrynus ing of ground structures in desert ants. J Exp Biol (Amblypygi: ) de Costa Rica. Rev Iber Arac- 209:3336–3344 nol 4:11–15 Shettleworth SJ (1998) Cognition, evolution, and behavior. Dittman A, Quinn T (1996) Homing in pacific salmon: Oxford University Press, New York Mechanisms and ecological basis. J Exp Biol 199:83–91 Spence AJ, Hebets EA (2007) Anatomy and physiology of Dyer FC (1998) Cognitive ecology of navigation. In: Dukas giant neurons in the antenniform leg of the amblypygid R (ed) Cognitive ecology: The evolutionary ecology of Phrynus marginemaculatus. J Arachnol 34:566–577 information processing and decision making. Univer- Warrant EJ, Kelbur A, Gislén A, Greiner B, Ribi W, Wcislo sity of Chicago Press, Chicago WT (2004) Nocturnal vision and landmark orientation Erber J, Kierzek S, Sander E, Grandy K (1998) Tactile learn- in a tropical halictid bee. Curr Biol 14:1309–1318 ing in the honeybee. J Comp Physiol A 183:737–744 Weygoldt P (1977) Coexistence of two species of whip spi- Foelix RF, Hebets EA (2001) Sensory biology of whip spi- ders (genus Heterophrynus) in the neotropical rain forest ders (Arachnida, Amblypygi). Andrias 15:129–140 (Arachnida, Amblypygi). Oecologia 27:363–370 Goyret J, Raguso RA (2006) The role of mechanosensory in- Weygoldt P (2000) Whip spiders (: Amblypygi). put in flower handling efficiency and learning by Man- Their biology, morphology and systematics. Apollo duca sexta. J Exp Biol 209:1585–1593 Books, Stenstrup Hebets EA (2002) Relating the unique sensory system of Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, amblypygids to the ecology and behavior of Phrynus Upper Saddle River parvulus from Costa Rica (Arachnida, Amblypygi). Can J Zool 80:286–295